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RAAF squadrons were permanently based at the Canberra Aerodrome from 1939. The base was formally established as RAAF Station Canberra on 1 April 1940. In 1941 part of the airport was named Fairbairn Airbase after the late Minister for Air and Civil Aviation James Fairbairn, Member of the Australian House of Representatives, who was killed in an aircraft crash in the proximity of the airfield on 13 August 1940. The first Netherlands East Indies Air Force squadron was 18 (NEI) Squadron, which was formed as an RAAF Squadron at Fairbairn airfield in Canberra on 4 April 1942 under the command of Lieutenant Colonel B.J. Fiedeldij. The Squadron was formed from the two groups of Dutch airmen at Archerfield and Melbourne. It flew North American B-25 Mitchells. The Squadron's Dutch personnel (and a few Javanese) were complemented by a number of RAAF personnel covering both aircrew and ground crew occupations. The base became Headquarters RAAF Canberra in 1952. In December 1960 the base was selected as the locality for the RAAF Staff College, and in 1962, the area was renamed RAAF Base Fairbairn.

The Defence Reform Program (DRP) determined the base was no longer required and on 28 May 1998 the lease on the base was sold to Canberra International Airport Pty Ltd.[1] Part of the base was sub-leased back to the Australian Department of Defence on a five-year lease to allow the progressive wind up of operations. The base was decommissioned on 27 June 2003 and the domestic area became known as Defence Establishment Fairbairn, with Canberra International Airport[2] and the Capital Airport Group[3] having full control of the airfield and the site.

The only remaining military unit is No. 34 Squadron RAAF, which is responsible for the operations of the RAAF's VIP transport aircraft that are used to transport Australian officials such as the Prime Minister, cabinet ministers, the Governor General, the leader of the opposition and high ranking defence force officers when travelling both internationally or within Australia.

Besides being the home base of No 34 Squadron's special purpose VIP BBJ1s and Bombardier Challenger 604s, Fairbairn is also regularly used by other defence force aircraft.

The airport is used by official aircraft carrying foreign heads of state or government when visiting Canberra, for example when the US President visits Canberra, Air Force One lands there.

Fairbairn was also home to No. 28 Squadron (Active Reserve Squadron) until it was relocated to HMAS Harman when Fairbairn was decommissioned.

In 2006, Canberra International Airport Pty Ltd, and the airport management company Capital Airport Group Pty Ltd, jointly released a prospectus[4] and embarked on a building program in the area now called "Fairbairn".[5] These new buildings have been leased and are occupied by the Department of Defence[6] and other tenants.